Lineage tracing with Axin2 reveals distinct developmental and adult populations of Wnt/β-catenin-responsive neural stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 18, 2013, Pages 7324-7329

  Bowmana, Angela N ^a,b,c   Van Amerongen, Renée ^a,b,d   Palmer, Theo D ^a   Nusse, Roeland ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Astrocyte; Forebrain; Radial glia cell

Indexed keywords

AXIN2 PROTEIN; BETA CATENIN; PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROGENY; SUBVENTRICULAR ZONE; WNT SIGNALING PATHWAY;

ADULT STEM CELLS; ANIMALS; ANIMALS, NEWBORN; AXIN PROTEIN; BETA CATENIN; CELL LINEAGE; DENTATE GYRUS; EMBRYO, MAMMALIAN; INTEGRASES; MICE; NEURAL STEM CELLS; NEUROGLIA; STAINING AND LABELING; TIME FACTORS; WNT SIGNALING PATHWAY;

MAMMALIA;

EID: 84876897705     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305411110     Document Type: Article

References (39)

1. Noctor SC, et al. (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22(8):3161-3173. (Pubitemid 35379204)
2. Anthony TE, Klein C, Fishell G, Heintz N (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41(6):881-890. (Pubitemid 38429732)
3. Mori T, Buffo A, Götz M (2005) The novel roles of glial cells revisited: The contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol 69:67-99. (Pubitemid 43588868)
4. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
5. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703-716. (Pubitemid 29278045)
6. Seri B, García-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21(18):7153-7160. (Pubitemid 32846963)
7. Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17(13):5046-5061. (Pubitemid 27263818)
8. Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978-981. (Pubitemid 26066393)
9. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo P-M (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6(5):507-518. (Pubitemid 36514699)
10. Alvarez-Buylla A, Lim DA (2004) For the long run: Maintaining germinal niches in the adult brain. Neuron 41(5):683-686. (Pubitemid 38326831)
11. Lai K, Kaspar BK, Gage FH, Schaffer DV (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6(1):21-27. (Pubitemid 36026328)
12. Lie D-C, et al. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437(7063):1370-1375. (Pubitemid 41568684)
13. Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149(6):1192-1205.
14. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127(3):469-480.
15. Michaelidis TM, Lie DC (2008) Wnt signaling and neural stem cells: Caught in the Wnt web. Cell Tissue Res 331(1):193-210. (Pubitemid 350265487)
16. Zechner D, et al. (2003) beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258(2):406-418. (Pubitemid 36686723)
17. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297(5580):365-369. (Pubitemid 34790759)
18. van Amerongen R, Bowman AN, Nusse R (2012) Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 11(3):387-400.
19. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluorescent Cre reporter mouse. Genesis 45(9):593-605. (Pubitemid 350013057)
20. Monuki ES, Porter FD, Walsh CA (2001) Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32(4):591-604. (Pubitemid 33145194)
21. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125(12):2315-2325. (Pubitemid 28336391)
22. Megason SG, McMahon AP (2002) A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129(9):2087-2098. (Pubitemid 34874223)
23. Backman M, et al. (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 279(1):155-168. (Pubitemid 40222176)
24. Junghans D, Hack I, Frotscher M, Taylor V, Kemler R (2005) Beta-catenin-mediated cell-adhesion is vital for embryonic forebrain development. Dev Dyn 233(2):528-539. (Pubitemid 40734052)
25. Gulacsi AA, Anderson SA (2008) Beta-catenin-mediated Wnt signaling regulates neurogenesis in the ventral telencephalon. Nat Neurosci 11(12):1383-1391.
26. Barolo S (2006) Transgenic Wnt/TCF pathway reporters: All you need is Lef? Oncogene 25(57):7505-7511.
27. Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437(7060):894-897. (Pubitemid 41486765)
28. Merkle FT, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101(50):17528-17532. (Pubitemid 39657437)
29. Young KM, Fogarty M, Kessaris N, Richardson WD (2007) Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci 27(31):8286-8296. (Pubitemid 47219615)
30. Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317(5836):381-384. (Pubitemid 47106379)
31. Moriyama A, et al. (2007) GFP transgenic mice reveal active canonical Wnt signal in neonatal brain and in adult liver and spleen. Genesis 45(2):90-100. (Pubitemid 46399464)
32. Piccin D, Morshead CM (2011) Wnt signaling regulates symmetry of division of neural stem cells in the adult brain and in response to injury. Stem Cells 29(3):528-538.
33. Craig CG, D'sa R, Morshead CM, Roach A, van der Kooy D (1999) Migrational analysis of the constitutively proliferating subependyma population in adult mouse forebrain. Neuroscience 93(3):1197-1206.
34. Cotsarelis G, Cheng SZ, Dong G, Sun TT, Lavker RM (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: Implications on epithelial stem cells. Cell 57(2):201-209. (Pubitemid 19112360)
35. Bondolfi L, Ermini F, Long JM, Ingram DK, Jucker M (2004) Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol Aging 25(3):333-340. (Pubitemid 38220969)
36. Tavazoie M, et al. (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3(3):279-288.
37. Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127(3):457-467. (Pubitemid 30093394)
38. Ihrie RA, et al. (2011) Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71(2):250-262.
39. Renault VM, et al. (2009) FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5(5):527-539.